Alena Stasenko1, Erik Kaestner1, Anny Reyes1, Sanam J Lalani1, Brianna Paul1, Manu Hegde1, Jonathan L Helm1, Sharona Ben-Haim1, Carrie R McDonald2. 1. From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA. 2. From the Center for Multimodal Imaging and Genetics (A.S., E.K., A.R., C.R.M.) and Departments of Psychiatry (A.S., E.K., A.R., S.J.L., C.R.M.) and Neurosurgery (S.B.-H.), University of California, San Diego; San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology (A.R., C.R.M.); Department of Neurology (B.P., M.H.), University of California, San Francisco; and Department of Psychology (J.L.H.), San Diego State University, CA. camcdonald@ucsd.edu.
Abstract
BACKGROUND AND OBJECTIVES: Risk for memory decline is a substantial concern in patients with temporal lobe epilepsy (TLE) undergoing anterior temporal lobectomy (ATL). Although prior studies have identified associations between memory and integrity of white matter (WM) networks within the medial temporal lobe (MTL) preoperatively, we contribute a study examining whether microstructural asymmetry of deep and superficial WM networks within the MTL predicts postoperative memory decline. METHODS: Patients with drug-resistant TLE were recruited from 2 epilepsy centers in a prospective longitudinal study. All patients completed preoperative T1 and diffusion-weighted MRI (DWI) as well as preoperative and postoperative neuropsychological testing. Preoperative fractional anisotropy (FA) of the WM directly beneath the neocortex (i.e., superficial WM [SWM]) and of deep WM tracts associated with memory were calculated. Asymmetry was calculated for hippocampal volume and FA of each WM tract or region and examined in linear and logistic regressions with preoperative to postoperative memory change as the primary outcome. RESULTS: Data were analyzed from 42 patients with TLE (19 left TLE [LTLE], 23 right TLE [RTLE]) who underwent ATL. Leftward FA asymmetry of the entorhinal SWM was associated with decline on prose and associative recall in LTLE, whereas leftward FA asymmetry of the uncinate fasciculus (UNC) was associated with decline on prose recall only. After controlling for preoperative memory score and hippocampal volume, leftward FA asymmetry of the entorhinal SWM uniquely contributed to decline in both prose and associative recall (β = -0.46; SE 0.14 and β = -0.68; SE 0.22, respectively) and leftward FA asymmetry of the UNC uniquely contributed to decline in prose recall (β = -0.31; SE 0.14). A model combining asymmetry of hippocampal volume and entorhinal FA correctly classified memory outcomes in 79% of patients with LTLE for prose (area under the curve [AUC] 0.89; sensitivity 82%; specificity 75%) and 81% of patients for associative (AUC 0.79; sensitivity 83%; specificity 80%) recall. Entorhinal SWM asymmetry was the strongest predictor in both models. DISCUSSION: Preoperative asymmetry of deep WM and SWM integrity within the MTL is a strong predictor of postoperative memory decline in TLE, suggesting that surgical decision-making may benefit from considering each patient's WM network adequacy and reserve in addition to hippocampal integrity. CLASSIFICATION OF EVIDENCE: This study provides Class II evidence that preoperative asymmetry of deep WM and SWM integrity within the MTL is a predictor of postoperative memory decline.
BACKGROUND AND OBJECTIVES: Risk for memory decline is a substantial concern in patients with temporal lobe epilepsy (TLE) undergoing anterior temporal lobectomy (ATL). Although prior studies have identified associations between memory and integrity of white matter (WM) networks within the medial temporal lobe (MTL) preoperatively, we contribute a study examining whether microstructural asymmetry of deep and superficial WM networks within the MTL predicts postoperative memory decline. METHODS: Patients with drug-resistant TLE were recruited from 2 epilepsy centers in a prospective longitudinal study. All patients completed preoperative T1 and diffusion-weighted MRI (DWI) as well as preoperative and postoperative neuropsychological testing. Preoperative fractional anisotropy (FA) of the WM directly beneath the neocortex (i.e., superficial WM [SWM]) and of deep WM tracts associated with memory were calculated. Asymmetry was calculated for hippocampal volume and FA of each WM tract or region and examined in linear and logistic regressions with preoperative to postoperative memory change as the primary outcome. RESULTS: Data were analyzed from 42 patients with TLE (19 left TLE [LTLE], 23 right TLE [RTLE]) who underwent ATL. Leftward FA asymmetry of the entorhinal SWM was associated with decline on prose and associative recall in LTLE, whereas leftward FA asymmetry of the uncinate fasciculus (UNC) was associated with decline on prose recall only. After controlling for preoperative memory score and hippocampal volume, leftward FA asymmetry of the entorhinal SWM uniquely contributed to decline in both prose and associative recall (β = -0.46; SE 0.14 and β = -0.68; SE 0.22, respectively) and leftward FA asymmetry of the UNC uniquely contributed to decline in prose recall (β = -0.31; SE 0.14). A model combining asymmetry of hippocampal volume and entorhinal FA correctly classified memory outcomes in 79% of patients with LTLE for prose (area under the curve [AUC] 0.89; sensitivity 82%; specificity 75%) and 81% of patients for associative (AUC 0.79; sensitivity 83%; specificity 80%) recall. Entorhinal SWM asymmetry was the strongest predictor in both models. DISCUSSION: Preoperative asymmetry of deep WM and SWM integrity within the MTL is a strong predictor of postoperative memory decline in TLE, suggesting that surgical decision-making may benefit from considering each patient's WM network adequacy and reserve in addition to hippocampal integrity. CLASSIFICATION OF EVIDENCE: This study provides Class II evidence that preoperative asymmetry of deep WM and SWM integrity within the MTL is a predictor of postoperative memory decline.
Authors: Yu-Hsuan A Chang; Nobuko Kemmotsu; Kelly M Leyden; N Erkut Kucukboyaci; Vicente J Iragui; Evelyn S Tecoma; Leena Kansal; Marc A Norman; Rachelle Compton; Tobin J Ehrlich; Vedang S Uttarwar; Anny Reyes; Brianna M Paul; Carrie R McDonald Journal: Brain Lang Date: 2017-04-20 Impact factor: 2.381
Authors: Donald J Hagler; Mazyar E Ahmadi; Joshua Kuperman; Dominic Holland; Carrie R McDonald; Eric Halgren; Anders M Dale Journal: Hum Brain Mapp Date: 2009-05 Impact factor: 5.038
Authors: Silvia B Bonelli; Robert H W Powell; Mahinda Yogarajah; Rebecca S Samson; Mark R Symms; Pamela J Thompson; Matthias J Koepp; John S Duncan Journal: Brain Date: 2010-02-15 Impact factor: 13.501
Authors: J T Langfitt; M Westerveld; M J Hamberger; T S Walczak; D V Cicchetti; A T Berg; B G Vickrey; W B Barr; M R Sperling; D Masur; S S Spencer Journal: Neurology Date: 2007-06-05 Impact factor: 9.910
Authors: M Yogarajah; H W R Powell; G J M Parker; D C Alexander; P J Thompson; M R Symms; P Boulby; C A Wheeler-Kingshott; G J Barker; M J Koepp; J S Duncan Journal: Neuroimage Date: 2008-01-10 Impact factor: 6.556